1. Manna Warburton & Gerry Closs
Downstream Spawning Migration in Amphidromous Fishes: A Link to Catadromy through Larval Transport
Manna Warburton & Gerry Closs
Dept. of Zoology, University of Otago
New Zealand
Torrentfish
Mike Joy
G. brevipinnis
Stella McQueen
G. huttoni
Hi everyone, my name’s Manna Warburton and I’m going to be presenting some work I did with Gerry Closs form the University of Otago, and I’m going to be talking about how downstream spawning migrations in amphidromous fishes form a link to catadromy through larval transport.
Bruno David

2. Amphidromy & Catadromy
Both diadromous life history strategies
Diverse range of taxa
Gobiidae, Cottidae, Galaxiiidae, Eleotridae, Prototroctes, Pinguipedidae, Retropinnidae, Kuhliidae, Bovichthyidae
Widespread geographical distribution
Indo-Pacific & Caribbean coastlines & islands
Typically (but not exclusively)
Relatively small species
High fecundity, with small eggs
Obligate pelagic larval stage
Before I get into it, I assume you’re all familiar with the form of diadromy that’s common in the northern hemisphere, which is anadromy, which is practiced by salmonids. Amphidromy and catadromy are the other two forms of diadromy, and they include a wide range of taxa and are common across much of the southern hemisphere, and are typically but not exclusively small bodied fish with high fecundity and an obligate pelagic larval stage.

3. Amphidromy & Catadromy
Fresh Water
Sea
Growth to adult
Pelagic larvae
Weeks to months
Post-larval to Juvenile Migration
Larval Migration
Spawning & rapid hatch
Adult
Amphidromy
Fresh Water
Sea
Growth to adult
Spawning
Adult migration to sea
Pelagic larvae
Weeks to months
Post-larval to Juvenile Migration
In amphidromous life histories, adults live and spawn in fresh water, and larvae undergo a rapid migration into the pelagic marine environment where they live and grow for some time before returning to freshwater to complete the lifecycle.
Adult
Catadromy

4. Amphidromy & Catadromy
Fresh Water
Sea
Growth to adult
Pelagic larvae
Weeks to months
Post-larval to Juvenile Migration
Larval Migration
Spawning & rapid hatch
Adult
Amphidromy
Key difference
Fresh Water
Sea
Growth to adult
Spawning
Adult migration to sea
Pelagic larvae
Weeks to months
Post-larval to Juvenile Migration
Catadromous life histories differ only in that adults perform a migration into the marine environment before spawning, with the other elements of the lifecycle being the same as amphidromous life histories
Adult
Catadromy

5. Amphidromy & Catadromy
Fresh Water
Sea
Growth to adult
Pelagic larvae
Weeks to months
Post-larval to Juvenile Migration
Larval Migration
Spawning & rapid hatch
Adult
Amphidromy
Near-catadromous
Mildly catadromous
Quasi-catadromous
Fresh Water
Sea
Growth to adult
Spawning
Adult migration to sea
Pelagic larvae
Weeks to months
Post-larval to Juvenile Migration
As more information has been collected about migratory behaviours, a suite of amphidromous fishes that perform downstream migrations prior to spawning has created some confusion about what category they belong in, and they’ve been referred to in the literature as “near catadromous” mildly catadromous and quasi-catadromous, so there’s some confusion about where they belong.
Adult
Catadromy

6. Why Amphidromy or Catadromy?
Gross
Proposed amphidromy transitional between anadromy & catadromy
Anadromy & catadromy transitional between marine & freshwater life histories
Direction of evolution related to relative productivity of marine & freshwater habitats
McDowall
Didn’t really consider catadromy extensively
Argued amphidromous life histories allow larval dispersal to new habitat
So why be amphidromous or catadromous for that matter? Why engage in migrations between freshwater and marine environments at a sensitive stage of development? Well Gross attempted to answer this is 1987 when he proposed that amphidromy was a transitional state between the other two diadromous life histories. He went on to postulate that anadromy and catadromy were themselves transitional states between non migratory marine and freshwater life histories, and that the direction of evolution was related to the relative productivity of the environments these animals were migrating between.
Bob McDowall, who is widely considered to be the father of amphidromous research in the southern hemisphere, argued that amphidromous life histories specifically allowed for dispersal into new habitats in species that lived in very isolated freshwater streams on tropical islands
Gross (1987) Am Fish Soc Symp; McDowall (2007) Fish & Fisheries

7. An Alternate View of Amphidromy (& Catadromy)
Closs, Hicks & Jellyman
A life history strategy that allows for high fecundity in (mostly) small fluvial fish species
Produce tiny larvae that must rear in pelagic environment, usually marine
Consequently, a life history restricted to species that can rapidly transport eggs or larvae to sea
Dispersal is an incidental but useful ‘by-product’
Small eggs allow for high fecundity
But limited resources (yolk) for larvae
Must rapidly complete migration from stream to sea before starvation occurs
So this year, Closs Hicks and Jellyman proposed an alternative explanation for the role of amphidromy, and I will argue that it fits catadromy as well. They think that amphidromy is a life history strategy that allows these small bodied fishes to boost their fecundity relative to non-migratory conspecifics by producing tiny pelagic larvae, and consequently, this is a life history that is restricted to species that can rapidly transport their eggs or larvae into the sea from the adult freshwater habitat. And dispersal ends up as a useful, but incedental biproduct of this strategy.
But there’s a catch, and that is that when you produce lots of small eggs, it leaves limited resources for individual larvae which are then prone to starvation if they don’t make it into the ocean rapidly enough.
Closs, Hicks & Jellyman (2013) Freshwater Biology

8. Amphidromy & Torrentfish
Endemic New Zealand amphidromous fish
Max length 150 mm, > 50,000 tiny eggs
Penetrates up to ~220 km inland in low gradient but fast flowing rivers & streams
How to get eggs/larvae to sea quickly?
Evidence for migration
Females upstream, males downstream
Suggested females must migrate to spawn
The species that I’m focusing on as part of my PhD research is the New Zealand torrentfish. It’s a fairly typical amphidromous fish in that it’s relatively small at 150mm but has very high fecundity, with ripe females holding between 30 and 50k eggs. It’s unusual in that it can occur up to 220km inland in lower gradient systems, and this poses the question. How is an obligate diadromous fish transporting its eggs 200km to the sea? Well there’s some evidence for migration in the species in the form of research showing that they’re sexually segregated, with the females living upstream and the males downstream, which would suggest that females must be migrating downstream to meet the males and spawn.
Bruno David
Scrimgeour & Eldon (1989) N Z J Mar Freshw Res

9. Aims Do torrentfish migrate downstream to spawn?
Torrentfish size & sex distribution across multiple rivers at varying distances inland
Monthly size / sex structure of torrentfish along Waianakarua River
So the aim of my study was to determine whether torrentfish were migrating downstream to spawn, and I did this by looking at size and sex distributions across multiple rivers at varying distances inland, as well as monitoring demographics monthly along a single river.

10. Methods Electrofishing of 21 sites in 12 South Island river systems
20 fish retained per sampling, dissected & sexed
Includes juveniles & adults
Longtitudinal monthly monitoring on Waianakarua River at four sites
Non-lethal sampling
Mature ripe fish sexed based on external appearance
My methods were fairly straightforward and we electrofished 21 sites in 12 rivers, keeping 20 fish per site, and we dissected these fish to determine their sex. At the monitoring site, we did catch and release monitoring, and sexed mature fish based on external characteristics.

11. Here’s an example of a ripe female torrentfish on the left and a male on the right, you could tell ripe males from females because they would express milt when handled.
Manna Warburton

12. Multi-River Study – Sex/Size vs Inland Penetration
Males
Juvenile grow as migrate inland
Progressive downstream migration at begins at maturity
Largest males located near river mouth
Prime spawning habitat?
So here’s what we found for male torrentfish in the multi-river group. Juveniles invade at about 30-40mm total length and steadily move inland as they grow, till they reach about 70mm, which is about the time they become sexually mature.

13. Multi-River Study – Sex/Size vs Inland Penetration
Males
Juvenile grow as migrate inland
Progressive downstream migration at begins at maturity
Largest males located near river mouth
Prime spawning habitat?
At this point they start heading back downstream, and we find the largest adult males at sites closest to the ocean, which is likely to be where the majority of spawning is taking place

14. Multi-River Study – Sex/Size vs Inland Penetration
Females
Juveniles grow as migrate inland
Mixed age / size downstream
Females migrating downstream at different ages or up and downstream?
Short period at spawning sites
The pattern for females is the same for juvenile fish

15. Multi-River Study – Sex/Size vs Inland Penetration
Females
Juveniles grow as migrate inland
Mixed age / size downstream
Females migrating downstream at different ages or up and downstream?
Short period at spawning sites
They grow and invade inland up to about 70mm

16. Multi-River Study – Sex/Size vs Inland Penetration
Females
Juveniles grow as migrate inland
Mixed age / size downstream
Females migrating downstream at different ages or up and downstream?
Short period at spawning sites
At this point they may be returning downstream at different ages

17. Multi-River Study – Sex/Size vs Inland Penetration
Females
Juveniles grow as migrate inland
Mixed age / size downstream
Females migrating downstream at different ages or up and downstream?
Short period at spawning sites
Or going downstream and spawning before migrating back upstream and then down again to spawn again, but whatever they’re doing, they don’t seem to be hanging around downstream

18. Monthly Size / Sex Distribution Study
Time (Julian Date)
Size (mm)
Upstream
Downstream
Waianakarua River
So here’s the data from the monthly demographic monitoring, with each of these box plots representing a visit to these two sites, which were an upstream site that was mostly female, and a downstream site that was mostly male.

19. Monthly Size / Sex Distribution Study
Time (Julian Date)
Size (mm)
Upstream
Downstream
Mostly ripe females
Waianakarua River
Mostly ripe males
Ripe males & females
What we saw was a cohort of large adult females become increasingly less common at this upper site, and become more common at the downstream site over the course of a single breeding season

20. Migration in Torrentfish
Torrentfish are migrating to spawn
Majority of spawning takes place in lower reaches
Spawning in downstream locations reduces larval migration times
Based on our sampling, we think that torrentfish are migrating to spawn, and that spawning is taking place in the lower reaches of the systems these fish occupy. And it’s our hypothesis that spawning in these downstream locations reduces both the distance and the time it takes for these very small larvae to reach the marine nursery habitat.

21. Downstream Migration in Amphidromous & Catadromous Fish
Pattern of downstream migration to spawn not unique to torrentfish
Common feature amongst amphidromous species that inhabit low gradient rivers
A potential strategy to reduce distance of downstream larval transport to sea
With near-catadromous & catadromous strategies being ‘extensions’ of this transport mechanism
When we look at other examples of migration in amphidromous fishes, we find that this is actually a common feature of species that specifically inhabit low gradient systems. Like I said before, we think that this is a strategy to reduce the time and distance larvae have to travel to reach the sea, and from here it’s not much further to migrate into the estuary, or the nearshore marine environment, and into a fully catadromous life history.

22. Amphidromy, Catadromy & River Gradient
Stream Gradient
Headwaters to Sea
Barrier
Steep & fast discharge to sea
Moderate inland penetration
Amphidromous with no down-stream migration
Transport relies entirely on larval drift
Many Galaxias, Gobiidae, Cottidae
Low gradient & fast discharge to sea
Considerable inland penetration
Amphidromous but with
migration downstream
Spawning in freshwater above estuary
Torrentfish, Awaous guamensis, Australian grayling, Ayu
Low gradient & slow discharge to sea
Considerable inland penetration
Near-catadromy or catadromy
Downstream migration to estuary or sea overcome barrier to passive transport
Galaxias maculatus, tupong, many others
When we look across the landscape at patterns of species distribution, we find amphidromous fishes with no downstream migration occupying steep, high gradient systems that afford rapid transport of larvae into the sea, and we find these species only a moderate distance inland. As gradient decreases, we find amphidromous fishes that engage in downstream migrations, and these species can often penetrate long distances inland. Finally as systems become extremely low gradient, with tidally influenced lower reaches, we see near catadromous and fully catadromous life histories dominating.

23. Conclusion
Propose that amphidromy & catadromy are functionally equivalent
Enables high fecundity by production of tiny pelagic larvae
But lowland barriers to larval transport increase as gradient & speed of discharge to sea declines
Requires increasing levels of ‘parental assistance’ for rapid transfer of larvae
Distribution of different strategies reflects response to coastal landscape & hydrology
So in conclusion, if you accept Closs’s interpretation of amphidromy, and by extension catadromy, as life histories associated with increasing fecundity through the production of tiny pelagic larvae, then the two life histories can be viewed as a single functionally equivalent strategy, where barriers to larval transport associated with gradient and discharge are mediated by increasing levels of parental assistance for the rapid transfer of larvae into the marine environment, with the distribution of different strategies being a response to coastal landscapes and hydrology

24. Thanks to Environment Southland Department of Conservation
University of Otago
Closs Lab
In closing I’d like to thank Environment Southland, the Department of Conservation, and the University of Otago, as well as my lab mates for their support in making this work possible